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Macrophyte Complexity Controls Nutrient Uptake in Lowland Streams

Abstract

Macrophytes act as ecosystem engineers in lowland stream ecosystems, enhancing habitat complexity and physical structure. Studies have demonstrated that macrophyte abundance and growth form can dictate the degree to which physical and biological stream characteristics are altered. However, few studies have investigated the influence of macrophytes and their species-specific variation in morphological complexity on functional processes, such as nutrient uptake. We injected 15N-labeled ammonium (15N-NH4 +) into four macrophyte-rich lowland streams in Denmark to quantify the uptake of NH4 + by macrophytes, epiphytic biofilms, benthic biofilms, and suspended particulate organic matter in the water column. Overall, macrophytes and their epiphytic biofilms accounted for 71–98% of the reach-weighted uptake across the study streams. While macrophytes had the highest rates of NH4 + uptake among the compartments we measured, the epiphytic biofilms had the highest uptake efficiency, ranging from 0.06 to 0.6 mg N mg N −1biomass d−1. Among all compartments, the uptake efficiency was inversely related to the carbon-to-nitrogen ratio. Macrophyte complexity, expressed as leaf perimeter-to-area ratio (P:A), varied among the five species found in the study streams. The uptake rates by macrophyte species with high leaf P:A were, on average, an order of magnitude higher than the rates for species with simple leaf morphology (430 vs. 49 mg N m−2 d−1). In summary, our results indicate that macrophytes regulate stream function both via direct uptake of NH4 + from the water column and by providing a substrate for epiphytic biofilms. Furthermore, the effect of leaf architecture on nutrient uptake rates provides evidence that physical complexity can enhance ecosystem function.

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References

  • APHA. 2005. Standard methods for the examination of water and wastewater. 20th edn. Washington: American Public Health Association.

    Google Scholar 

  • Baattrup-Pedersen A, Larsen SE, Riis T. 2003. Composition and richness of macrophyte communities in small Danish streams: influence of environmental factors and weed cutting. Hydrobiologia 495:171–9.

    Article  Google Scholar 

  • Baattrup-Pedersen A, Kristensen EA, Jørgensen J, Skriver J, Kronvang B, Andersen HE, Hoffman CC, Kjellerup Larsen LM. 2009. Can a priori defined reference criteria be used to select reference sites in Danish streams? Implications for implementing the Water Framework Directive. J Environ Monit 11:344–52.

    Article  CAS  PubMed  Google Scholar 

  • Battin TJ, Kaplan LA, Newbold JD, Cheng X, Hansen C. 2003. Effects of current velocity on the nascent architecture of stream microbial biofilms. Appl Environ Microbiol 69:5443–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell N, Riis T, Suren AM, Baattrup-Pedersen A. 2013. Distribution of invertebrates within beds of two morphologically contrasting stream macrophyte species. Fundam Appl Limnol 183:309–21.

    Article  Google Scholar 

  • Bernot MJ, Dodds WK. 2005. Nitrogen retention, removal, and saturation in lotic ecosystems. Ecosystems 8:442–53.

    Article  CAS  Google Scholar 

  • Bernot MJ, Tank JL, Royer TV, David MB. 2006. Nutrient uptake in streams draining agricultural catchments of the midwestern United States. Freshw Biol 51:499–509.

    Article  CAS  Google Scholar 

  • Bouchard V, Frey SD, Gilbert JM, Reed SE. 2007. Effects of macrophyte functional group richness on emergent freshwater wetland functions. Ecology 88:2903–14.

    Article  PubMed  Google Scholar 

  • Bouma TJ, De Vries MB, Herman PMJ. 2010. Comparing ecosystem engineering efficiency of two plant species with contrasting growth strategies. Ecology 91:2696–704.

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR. 2002. Model selection and multi-model inference: a practical information-theoretical approach. New York: Springer.

    Google Scholar 

  • Caraco N, Cole J, Findlay S, Wigand C. 2006. Vascular plants as engineers of oxygen in aquatic systems. Bioscience 56:219–25.

    Article  Google Scholar 

  • Carignan R. 1982. An empirical model to estimate the relative importance of roots in phosphorus uptake by aquatic macrophytes. Can J Fish Aquat Sci 39:243–7.

    Article  CAS  Google Scholar 

  • Carignan R, Kalff J. 1982. Phosphorus release by submerged macrophytes: significance to epiphyton and phytoplankton. Limnol Oceanogr 27:419–27.

    Article  CAS  Google Scholar 

  • Cedergreen N, Madsen TV. 2003. Nitrate reductase activity in roots and shoots of aquatic macrophytes. Aquat Bot 76:203–12.

    Article  CAS  Google Scholar 

  • Chambers PA, Prepas EE, Bothwell ML, Hamilton HR. 1989. Roots versus shoots in nutrient uptake by aquatic macrophytes in flowing waters. Can J Fish Aquat Sci 46:435–9.

    Article  Google Scholar 

  • Cheruvelil KS, Soranno PA, Madsen JD, Roberson MJ. 2002. Plant architecture and epiphytic macroinvertebrate communities: the role of an exotic dissected macrophyte. J N Am Benthol Soc 21:261–77.

    Article  Google Scholar 

  • Davis JC, Minshall GW. 1999. Nitrogen and phosphorus uptake in two Idaho (USA) headwater wilderness streams. Oecologia 119:247–55.

    Article  Google Scholar 

  • Desmet NJS, Van Belleghem S, Seuntjens P, Bouma TJ, Buis K, Meire P. 2011. Quantification of the impact of macrophytes on oxygen dynamics and nitrogen retention in a vegetated lowland river. Phys Chem Earth 36:479–89.

    Article  Google Scholar 

  • Dodds WK, Biggs BJF. 2002. Water velocity attenuation by stream periphyton and macrophytes in relation to growth form and architecture. J N Am Benthol Soc 21:2–15.

    Article  Google Scholar 

  • Dodds WK, Martí E, Tank JL, Pontius J, Hamilton SK, Grimm NB, Bowden WB, McDowell WH, Peterson BJ, Valett HM, Webster JR, Gregory S. 2004. Carbon and nitrogen stoichiometry and nitrogen cycling rates in streams. Oecologia 140:458–67.

    Article  PubMed  Google Scholar 

  • Engelhardt KAM, Ritchie ME. 2002. The effect of aquatic plant species richness on wetland ecosystem processes. Ecology 83:2911–24.

    Article  Google Scholar 

  • Feijoó C, Giorgi A, Ferreiro N. 2011. Phosphate uptake in a macrophyte-rich Pampean stream. Limnologica 41:285–9.

    Article  Google Scholar 

  • Ferreiro N, Giorgi A, Feijoó C. 2013. Effects of macrophyte architecture and leaf shape complexity on structural parameters of the epiphytic algal community in a Pampean stream. Aquat Ecol 47:389–401.

    Article  Google Scholar 

  • Gordon ND, McMahon TA, Finlayson BL, Gippel CJ, Nathan RJ. 2004. Stream hydrology: an introduction for ecologists. 2nd edn. West Sussex: John Wiley and Sons Ltd.

    Google Scholar 

  • Gutierrez JL, Jones CG. 2006. Physical ecosystem engineers as agents of biogeochemical heterogeneity. Bioscience 56:227–36.

    Article  Google Scholar 

  • Hall RO, Tank JL, Sobota DJ, Mulholland PJ, Jonathan M, Brien O, Dodds WK, Webster JR, Valett HM, Poole GC, Bruce J, Meyer JL, Mcdowell WH, Johnson SL, Hamilton SK, Grimm B, Gregory SV, Dahm CN, Cooper LW, Ashkenas LR, Thomas M, Sheibley RW, Potter JD, Niederlehner BR, Johnson LT, Helton M, Crenshaw CM, Burgin AJ, Bernot MJ, Beaulieu JJ, Arango CP. 2009. Nitrate removal in stream ecosystems measured by Total uptake 15 N addition experiments. Limnol Oceanogr 54:653–65.

    Article  CAS  Google Scholar 

  • Hein M, Pedersen MF, Sand Jensen K. 1995. Size-dependent nitrogen uptake in micro- and macroalgae. Mar Ecol Prog Ser 118:247–54.

    Article  Google Scholar 

  • Hoellein TJ, Tank JL, Rosi-Marshall EJ, Entrekin SA, Lamberti GA. 2007. Controls on spatial and temporal variation of nutrient uptake in three Michigan headwater streams. Limnol Oceanogr 52:1964–77.

    Article  CAS  Google Scholar 

  • Holmes RM, McClelland JW, Sigman DM, Fry B, Peterson BJ. 1998. Measuring 15 N-NH4+ in marine, estuarine and fresh waters: an adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60:235–43.

    Article  CAS  Google Scholar 

  • Johnson LT, Tank JL, Arango CP. 2009. The effect of land use on dissolved organic carbon and nitrogen uptake in streams. Freshw Biol 54:2335–50.

    Article  CAS  Google Scholar 

  • Jones CG, Lawton JH, Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69:373–86.

    Article  Google Scholar 

  • Kaplan L, Bott T. 1989. Diel fluctuations in bacterial-activity on streambed substrata during vernal algal blooms—effects of temperature, water chemistry, and habitat. Limnol Oceanogr 34:718–33.

    Article  CAS  Google Scholar 

  • Kovalenko K, Thomaz S, Warfe D. 2012. Habitat complexity: approaches and future directions. Hydrobiologia 685:1–17.

    Article  Google Scholar 

  • Madsen TV, Cedergreen N. 2002. Sources of nutrients to rooted submerged macrophytes growing in a nutrient-rich stream. Freshw Biol 47:283–91.

    Article  Google Scholar 

  • Moeslund B, Løjtnant B, Mathiesen H, Mathiesen L, Pedersen A, Thyssen N, Schou JC. 1990. Danske vandplanter. Copenhagen: The Danish Environmental Protection Agency (DMU).

    Google Scholar 

  • Mulholland PJ, Tank JL, Sanzone DM, Wollheim WM, Peterson BJ, Webster JR, Meyer JL. 2000. Nitrogen cycling in a forest stream determined by a N-15 tracer addition. Ecol Monogr 70:471–93.

    Google Scholar 

  • Mulholland PJ, Tank JL, Webster JR, Bowden WB, Dodds WK, Gregory SV, Grimm NB, Hamilton SK, Johnson SL, Martí E, McDowell WH, Merriam JL, Meyer JL, Peterson BJ, Valett HM, Wollheim WM. 2002. Can uptake length in streams be determined by nutrient addition experiments? Results from an interbiome comparison study. J N Am Benthol Soc 21:544–60.

    Article  Google Scholar 

  • Newbold JD, Elwood JW, O’Neill RV, Van Winkle W. 1981. Measuring nutrient spiralling in streams. Can J Fish Aquat Sci 38:860–3.

    Article  Google Scholar 

  • O’Brien JM, Lessard JL, Plew D, Graham SE, McIntosh AR. 2014. Aquatic macrophytes alter metabolism and nutrient cycling in lowland streams. Ecosystems 17:405–17.

    Article  Google Scholar 

  • Peipoch M, Gacia E, Blesa A, Ribot M, Riera JL, Martí E. 2014. Contrasts among macrophyte riparian species in their use of stream water nitrate and ammonium: insights from 15 N natural abundance. Aquat Sci 76:203–15.

    Article  CAS  Google Scholar 

  • Rattray MR, Howard-Williams C, Brown JMA. 1991. Sediment and water as sources of nitrogen and phosphorus for submerged rooted aquatic macrophytes. Aquat Bot 40:225–37.

    Article  Google Scholar 

  • Riis T, Dodds WK, Kristensen PB, Baisner AJ. 2012. Nitrogen cycling and dynamics in a macrophyte-rich stream as determined by a release. Freshw Biol 57:1579–91.

    Article  CAS  Google Scholar 

  • Roberts BJ, Mulholland PJ. 2007. In-stream biotic control on nutrient biogeochemistry in a forested stream, West Fork of Walker Branch. J Geophys Res 112:G04002.

    Google Scholar 

  • Salehin M, Packman AI, Wörman A. 2003. Comparison of transient storage in vegetated and unvegetated reaches of a small agricultural stream in Sweden: seasonal variation and anthropogenic manipulation. Adv Water Resour 26:951–64.

    Article  Google Scholar 

  • Sand-Jensen K. 1998. Influence of submerged macrophytes on sediment composition and near-bed flow in lowland streams. Freshw Biol 39:663–79.

    Article  Google Scholar 

  • Sand-Jensen K, Andersen K, Andersen T. 1999. Dynamic properties of recruitment, expansion and mortality of macrophyte patches in streams. Int Rev Hydrobiol 84:497–508.

    Google Scholar 

  • Sigman DM, Altabet MA, Michener R, McCorkle DC, Fry B, Holmes RM. 1997. Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar Chem 57:227–42.

    Article  CAS  Google Scholar 

  • Simon KS, Niyogi DK, Frew RD, Townsend CR. 2007. Nitrogen dynamics in grassland streams along a gradient of agricultural development. Limnol Oceanogr 52:1246–57.

    Article  CAS  Google Scholar 

  • Stream Solute Workshop. 1990. Concepts and methods for assessing solute dynamics in stream ecosystems. J N Am Benthol Soc 9:95–119.

    Article  Google Scholar 

  • Thomaz SM, Dibble ED, Evangelista LR, Higuti J, Bini LM. 2008. Influence of aquatic macrophyte habitat complexity on invertebrate abundance and richness in tropical lagoons. Freshw Biol 53:358–67.

    Google Scholar 

  • Webster JR, Mulholland PJ, Tank JL, Valett HM, Dodds WK, Peterson BJ, Bowden WB, Dahm CN, Findlay S, Gregory SV, Grimm NB, Hamilton SK, Johnson SL, Martí E, McDowell WH, Meyer JL, Morrall DD, Thomas SA, Wollheim WM. 2003. Factors affecting ammonium uptake in streams: an inter-biome perspective. Freshw Biol 48:1329–52.

    Article  CAS  Google Scholar 

  • Wiegleb G, Bröring U, Filetti M, Brux H, Herr W. 2014. Long-term dynamics of macrophyte dominance and growth-form types in two north-west German lowland streams. Freshw Biol 59:1012–25.

    Article  Google Scholar 

  • Zar JH. 2009. Biostatistical analysis. 4th edn. Upper Saddle River: Prentice-Hall.

    Google Scholar 

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Acknowledgments

Our research was possible because of the technical and field support provided by Camilla HÃ¥kansson, Lone Ottosen, Birgitte Tagesen, and Ole Zahrtmann. We would also like to thank Walter Dodds and Jennifer Tank for their valuable insight, Ali Mikulyuk for comments on an earlier version of this manuscript, and Jesse Nippert and Troy Ocheltree at Kansas State University for processing our stable isotope samples. We are grateful to the Danish Council for Independent Research and the EU MARS Project (Contract #60337) for providing funding to support our research and the kind land owners who allowed us to access our field sites.

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Correspondence to Peter S. Levi.

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PSL helped design the study, performed the research, analyzed the data, and wrote the paper; TR conceived of and helped design the study, helped perform the research, and assisted in writing the paper; ABA helped perform the research and provided extensive revisions on the manuscript; MP helped perform the research and provided extensive revisions on the manuscript; KM helped perform the research and provided revisions to the paper; CB helped perform the research, conducted the GIS analysis, and provided revisions to the paper; ABP conceived of and helped design the study and assisted in writing the paper.

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Levi, P.S., Riis, T., Alnøe, A.B. et al. Macrophyte Complexity Controls Nutrient Uptake in Lowland Streams. Ecosystems 18, 914–931 (2015). https://doi.org/10.1007/s10021-015-9872-y

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